The role of histone demethylases in cancer therapy

Molecular Oncology

Volumn 6, Issue 6, 2012, Pages 683-703

  Hoffmann, Inga ^a   Roatsch, Martin ^a   Schmitt, Martin L ^a   Carlino, Luca ^b   Pippel, Martin ^b   Sippl, Wolfgang ^b   Jung, Manfred ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

Epigenetics; Histone demethylases; JMJC; LSD1; Lysine demethylase

Indexed keywords

(S) 2 HYDROXYGLUTARIC ACID; 2 HYDROXYGLUTARIC ACID; 2,4 PYRIDINEDICARBOXYLIC ACID; AZACITIDINE; BETA LAPACHONE; BIGUANIDE DERIVATIVE; BISBIGUANIDE DERIVATIVE; CARBIDOPA; CBB 1007; CLORGYLINE; DIMETHYL N OXALYLGLYCINE; DISULFIRAM DERIVATIVE; DOPAMINE; ENZYME INHIBITOR; FENCLONINE; HISTONE DEMETHYLASE; HISTONE METHYLTRANSFERASE; N OXALYL D TYROSINE DERIVATIVE; N OXALYLGLYCINE; N OXALYLGLYCINE DERIVATIVE; NAMOLINE; PARGYLINE; PG 11144; PG 11150; PHENELZINE; PYRIDINE 2,4 DICARBOXYLIC ACID DERIVATIVE; RETINOIC ACID; SMALL MOLECULE TRANSPORT AGENT; TRANYLCYPROMINE; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ANTINEOPLASTIC ACTIVITY; BIOCHEMISTRY; CANCER THERAPY; DRUG DESIGN; DRUG MECHANISM; DRUG STRUCTURE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME STRUCTURE; EPIGENETICS; HISTONE METHYLATION; HUMAN; MOLECULARLY TARGETED THERAPY; NONHUMAN; PRIORITY JOURNAL; REVIEW;

EID: 84869871771     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2012.07.004     Document Type: Review

References (148)

1. Adamo A., Sese B., Boue S., Castano J., Paramonov I., Barrero M.J., Izpisua Belmonte J.C. LSD1 regulates the balance between self-renewal and differentiation in human embryonic stem cells. Nat. Cell. Biol. 2011, 13:652-659.
2. Agger K., Christensen J., Cloos P.A., Helin K. The emerging functions of histone demethylases. Curr. Opin. Genet. Dev. 2008, 18:159-168.
3. Albert M., Helin K. Histone methyltransferases in cancer. Semin. Cell. Dev. Biol. 2010, 21:209-220.
4. Anand R., Marmorstein R. Structure and mechanism of lysine-specific demethylase enzymes. J. Biol. Chem. 2007, 282:35425-35429.
5. Anderton J.A., Bose S., Vockerodt M., Vrzalikova K., Wei W., Kuo M., Helin K., Christensen J., Rowe M., Murray P.G., Woodman C.B. The H3K27me3 demethylase, KDM6B, is induced by Epstein-Barr virus and over-expressed in Hodgkin's Lymphoma. Oncogene 2011, 30:2037-2043.
6. Aravind L., Iyer L.M. The SWIRM domain: a conserved module found in chromosomal proteins points to novel chromatin-modifying activities. Genome. Biol. 2002, 3. Research 0039.
7. Arrowsmith C.H., Bountra C., Fish P.V., Lee K., Schapira M. Epigenetic protein families: a new frontier for drug discovery. Nat. Rev. Drug Discov. 2012, 11:384-400.
8. Bannister A.J., Zegerman P., Partridge J.F., Miska E.A., Thomas J.O., Allshire R.C., Kouzarides T. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 2001, 410:120-124.
9. Baron R., Binda C., Tortorici M., McCammon J.A., Mattevi A. Molecular mimicry and ligand recognition in binding and catalysis by the histone demethylase LSD1-CoREST complex. Structure 2011, 19:212-220.
10. Benelkebir H., Hodgkinson C., Duriez P.J., Hayden A.L., Bulleid R.A., Crabb S.J., Packham G., Ganesan A. Enantioselective synthesis of tranylcypromine analogues as lysine demethylase (LSD1) inhibitors. Bioorg. Med. Chem. 2011, 19:3709-3716.
11. Binda C., Li M., Hubalek F., Restelli N., Edmondson D.E., Mattevi A. Insights into the mode of inhibition of human mitochondrial monoamine oxidase B from high-resolution crystal structures. Proc. Natl. Acad. Sci. U S A 2003, 100:9750-9755.
12. Binda C., Valente S., Romanenghi M., Pilotto S., Cirilli R., Karytinos A., Ciossani G., Botrugno O.A., Forneris F., Tardugno M., Edmondson D.E., Minucci S., Mattevi A., Mai A. Biochemical, structural, and biological evaluation of tranylcypromine derivatives as inhibitors of histone demethylases LSD1 and LSD2. J. Am. Chem. Soc. 2010, 132:6827-6833.
13. Bissinger E.M., Heinke R., Sippl W., Jung M. Histone methyltransferase inhibitors. Med. Chem. Commun. 2010, 1:114-124.
14. Brasacchio D., Okabe J., Tikellis C., Balcerczyk A., George P., Baker E.K., Calkin A.C., Brownlee M., Cooper M.E., El-Osta A. Hyperglycemia induces a dynamic cooperativity of histone methylase and demethylase enzymes associated with gene-activating epigenetic marks that coexist on the lysine tail. Diabetes 2009, 58:1229-1236.
15. Chang B., Chen Y., Zhao Y., Bruick R.K. JMJD6 is a histone arginine demethylase. Science 2007, 318:444-447.
16. Chang K.H., King O.N., Tumber A., Woon E.C., Heightman T.D., McDonough M.A., Schofield C.J., Rose N.R. Inhibition of histone demethylases by 4-carboxy-2,2'-bipyridyl compounds. Chem. Med. Chem. 2011, 6:759-764.
17. Chang P.C., Fitzgerald L.D., Hsia D.A., Izumiya Y., Wu C.Y., Hsieh W.P., Lin S.F., Campbell M., Lam K.S., Luciw P.A., Tepper C.G., Kung H.J. Histone demethylase JMJD2A regulates Kaposi's sarcoma-associated herpes virus replication and is targeted by a viral transcriptional factor. J. Virol. 2011, 85:3283-3293.
18. Chen H., Giri N.C., Zhang R., Yamane K., Zhang Y., Maroney M., Costa M. Nickel ions inhibit histone demethylase JMJD1A and DNA repair enzyme ABH2 by replacing the ferrous iron in the catalytic centers. J. Biol. Chem. 2010, 285:7374-7383.
19. Chen Y., Yang Y., Wang F., Wan K., Yamane K., Zhang Y., Lei M. Crystal structure of human histone lysine-specific demethylase 1 (LSD1). Proc. Natl. Acad. Sci. U S A 2006, 103:13956-13961.
20. Chen Z., Zang J., Whetstine J., Hong X., Davrazou F., Kutateladze T.G., Simpson M., Mao Q., Pan C.-H., Dai S., Hagman J., Hansen K., Shi Y., Zhang G. Structural insights into histone demethylation by JMJD2 family members. Cell 2006, 125:691-702.
21. Christensen J., Agger K., Cloos P.A.C., Pasini D., Rose S., Sennels L., Rappsilber J., Hansen K.H., Salcini A.E., Helin K. RBP2 belongs to a family of demethylases, specific for tri-and dimethylated lysine 4 on histone 3. Cell 2007, 128:1063-1076.
22. Clausen R.P., Pedersen M.T., Helin K. Histone demethylases. Epigenetic Targets in Drug Discovery 2009, 269-290. Wiley-VCH, Weinheim. W. Sippl, M. Jung (Eds.).
23. Clifton I.J., McDonough M.A., Ehrismann D., Kershaw N.J., Granatino N., Schofield C.J. Structural studies on 2-oxoglutarate oxygenases and related double-stranded beta-helix fold proteins. J. Inorg. Biochem. 2006, 100:644-669.
24. Cloos P.A., Christensen J., Agger K., Maiolica A., Rappsilber J., Antal T., Hansen K.H., Helin K. The putative oncogene GASC1 demethylates tri- and dimethylated lysine 9 on histone H3. Nature 2006, 442:307-311.
25. Couture J.F., Collazo E., Ortiz-Tello P.A., Brunzelle J.S., Trievel R.C. Specificity and mechanism of JMJD2A, a trimethyllysine-specific histone demethylase. Nat. Struct. Mol. Biol. 2007, 14:689-695.
26. Eissenberg J.C., Lee M.G., Schneider J., Ilvarsonn A., Shiekhattar R., Shilatifard A. The trithorax-group gene in Drosophila little imaginal discs encodes a trimethylated histone H3 Lys4 demethylase. Nat. Struct. Mol. Biol. 2007, 14:344-346.
27. Fodor B.D., Kubicek S., Yonezawa M., O'Sullivan R.J., Sengupta R., Perez-Burgos L., Opravil S., Mechtler K., Schotta G., Jenuwein T. Jmjd2b antagonizes H3K9 trimethylation at pericentric heterochromatin in mammalian cells. Genes Dev. 2006, 20:1557-1562.
28. Forneris F., Battaglioli E., Mattevi A., Binda C. New roles of flavoproteins in molecular cell biology: histone demethylase LSD1 and chromatin. FEBS J. 2009, 276:4304-4312.
29. Forneris F., Binda C., Adamo A., Battaglioli E., Mattevi A. Structural basis of LSD1-CoREST selectivity in histone H3 recognition. J. Biol. Chem. 2007, 282:20070-20074.
30. Garcia-Bassets I., Kwon Y.S., Telese F., Prefontaine G.G., Hutt K.R., Cheng C.S., Ju B.G., Ohgi K.A., Wang J., Escoubet-Lozach L., Rose D.W., Glass C.K., Fu X.D., Rosenfeld M.G. Histone methylation-dependent mechanisms impose ligand dependency for gene activation by nuclear receptors. Cell 2007, 128:505-518.
31. Guibourt, N., 2010. Phenylcyclopropylamine derivatives and their medical use. International Patent, WO2010/084160.
32. Guo X., Shi M., Sun L., Wang Y., Gui Y., Cai Z., Duan X. The expression of histone demethylase JMJD1A in renal cell carcinoma. Neoplasma 2011, 58:153-157.
33. Hamada S., Kim T.D., Suzuki T., Itoh Y., Tsumoto H., Nakagawa H., Janknecht R., Miyata N. Synthesis and activity of N-oxalylglycine and its derivatives as Jumonji C-domain-containing histone lysine demethylase inhibitors. Bioorg. Med. Chem. Lett. 2009, 19:2852-2855.
34. Hamada S., Suzuki T., Mino K., Koseki K., Oehme F., Flamme I., Ozasa H., Itoh Y., Ogasawara D., Komaarashi H., Kato A., Tsumoto H., Nakagawa H., Hasegawa M., Sasaki R., Mizukami T., Miyata N. Design, synthesis, enzyme-inhibitory activity, and effect on human cancer cells of a novel series of Jumonji domain-containing protein 2 histone demethylase inhibitors. J. Med. Chem. 2010, 53:5629-5638.
35. Harris W.J., Huang X., Lynch J.T., Spencer G.J., Hitchin J.R., Li Y., Ciceri F., Blaser J.G., Greystoke B.F., Jordan A.M., Miller C.J., Ogilvie D.J., Somervaille T.C. The histone demethylase KDM1A sustains the oncogenic potential of MLL-AF9 leukemia stem cells. Cancer Cell 2012, 21:473-487.
36. Hausinger R.P. FeII/alpha-ketoglutarate-dependent hydroxylases and related enzymes. Crit. Rev. Biochem. Mol. Biol. 2004, 39:21-68.
37. Hayami S., Kelly J.D., Cho H.S., Yoshimatsu M., Unoki M., Tsunoda T., Field H.I., Neal D.E., Yamaue H., Ponder B.A., Nakamura Y., Hamamoto R. Overexpression of LSD1 contributes to human carcinogenesis through chromatin regulation in various cancers. Int. J. Cancer 2011, 128:574-586.
38. Helias C., Struski S., Gervais C., Leymarie V., Mauvieux L., Herbrecht R., Lessard M. Polycythemia vera transforming to acute myeloid leukemia and complex abnormalities including 9p homogeneously staining region with amplification of MLLT3, JMJD2C, JAK2, and SMARCA2. Cancer Genet. Cytogen. 2008, 180:51-55.
39. Henikoff S., Shilatifard A. Histone modification: cause or cog?. Trends Genet. 2011, 27:389-396.
40. Hillringhaus L., Yue W.W., Rose N.R., Ng S.S., Gileadi C., Loenarz C., Bello S.H., Bray J.E., Schofield C.J., Oppermann U. Structural and evolutionary basis for the dual substrate selectivity of human KDM4 histone demethylase family. J. Biol. Chem. 2011, 286:41616-41625.
41. Horton J.R., Upadhyay A.K., Hashimoto H., Zhang X., Cheng X. Structural basis for human PHF2 Jumonji domain interaction with metal ions. J. Mol. Biol. 2011, 406:1-8.
42. Horton J.R., Upadhyay A.K., Qi H.H., Zhang X., Shi Y., Cheng X. Enzymatic and structural insights for substrate specificity of a family of jumonji histone lysine demethylases. Nat. Struct. Mol. Biol. 2009, 17:38-43.
43. Hou H., Yu H. Structural insights into histone lysine demethylation. Curr. Opin. Struct. Biol. 2010, 20:739-748.
44. Hu Q., Kwon Y.S., Nunez E., Cardamone M.D., Hutt K.R., Ohgi K.A., Garcia-Bassets I., Rose D.W., Glass C.K., Rosenfeld M.G., Fu X.D. Enhancing nuclear receptor-induced transcription requires nuclear motor and LSD1-dependent gene networking in interchromatin granules. Proc. Natl. Acad. Sci. U S A 2008, 105:19199-19204.
45. Huang J., Sengupta R., Espejo A.B., Lee M.G., Dorsey J.A., Richter M., Opravil S., Shiekhattar R., Bedford M.T., Jenuwein T., Berger S.L. p53 is regulated by the lysine demethylase LSD1. Nature 2007, 449:105-U180.
46. Huang Y., Greene E., Murray Stewart T., Goodwin A.C., Baylin S.B., Woster P.M., Casero R.A. Inhibition of lysine-specific demethylase 1 by polyamine analogues results in reexpression of aberrantly silenced genes. Proc. Natl. Acad. Sci. U S A 2007, 104:8023-8028.
47. Huang Y., Stewart T.M., Wu Y., Baylin S.B., Marton L.J., Perkins B., Jones R.J., Woster P.M., Casero R.A. Novel oligoamine analogues inhibit lysine-specific demethylase 1 and induce reexpression of epigenetically silenced genes. Clin. Cancer Res. 2009, 15:7217-7228.
48. Italiano A., Attias R., Aurias A., Perot G., Burel-Vandenbos F., Otto J., Venissac N., Pedeutour F. Molecular cytogenetic characterization of a metastatic lung sarcomatoid carcinoma: 9p23 neocentromere and 9p23-p24 amplification including JAK2 and JMJD2C. Cancer Genet. Cytogen. 2006, 167:122-130.
49. Ivan M., Haberberger T., Gervasi D.C., Michelson K.S., Gunzler V., Kondo K., Yang H., Sorokina I., Conaway R.C., Conaway J.W., Kaelin W.G. Biochemical purification and pharmacological inhibition of a mammalian prolyl hydroxylase acting on hypoxia-inducible factor. Proc. Natl. Acad. Sci. U S A 2002, 99:13459-13464.
50. Iwase S., Lan F., Bayliss P., de la Torre-Ubieta L., Huarte M., Qi H.H., Whetstine J.R., Bonni A., Roberts T.M., Shi Y. The X-linked mental retardation gene SMCX/JARID1C defines a family of histone H3 lysine 4 demethylases. Cell 2007, 128:1077-1088.
51. Kahl P., Gullotti L., Heukamp L.C., Wolf S., Friedrichs N., Vorreuther R., Solleder G., Bastian P.J., Ellinger J., Metzger E., Schule R., Buettner R. Androgen receptor coactivators lysine-specific histone demethylase 1 and four and a half LIM domain protein 2 predict risk of prostate cancer recurrence. Cancer Res. 2006, 66:11341-11347.
52. Karytinos A., Forneris F., Profumo A., Ciossani G., Battaglioli E., Binda C., Mattevi A. A novel mammalian flavin-dependent histone demethylase. J. Biol. Chem. 2009, 284:17775-17782.
53. Kauffman E.C., Robinson B.D., Downes M.J., Powell L.G., Lee M.M., Scherr D.S., Gudas L.J., Mongan N.P. Role of androgen receptor and associated lysine-demethylase coregulators, LSD1 and JMJD2A, in localized and advanced human bladder cancer. Mol. Carcinogen 2011, 50:931-944.
54. Kawazu M., Saso K., Tong K.I., McQuire T., Goto K., Son D.O., Wakeham A., Miyagishi M., Mak T.W., Okada H. Histone demethylase JMJD2B functions as a co-factor of estrogen receptor in breast cancer proliferation and mammary gland development. PLoS ONE 2011, 6:e17830.
55. Kim T.D., Oh S., Shin S., Janknecht R. Regulation of tumor suppressor p53 and HCT116 cell physiology by histone demethylase JMJD2D/KDM4D. PLoS ONE 2012, 7:e34618.
56. King O.N., Li X.S., Sakurai M., Kawamura A., Rose N.R., Ng S.S., Quinn A.M., Rai G., Mott B.T., Beswick P., Klose R.J., Oppermann U., Jadhav A., Heightman T.D., Maloney D.J., Schofield C.J., Simeonov A. Quantitative high-throughput screening identifies 8-hydroxyquinolines as cell-active histone demethylase inhibitors. PLoS ONE 2010, 5:e15535.
57. Klose R.J., Gardner K.E., Liang G., Erdjument-Bromage H., Tempst P., Zhang Y. Demethylation of histone H3K36 and H3K9 by Rph1: a Vestige of an H3K9 methylation system in Saccharomyces cerevisiae?. Mol. Cell. Biol. 2007, 27:3951-3961.
58. Klose R.J., Kallin E.M., Zhang Y. JmjC-domain-containing proteins and histone demethylation. Nat. Rev. Genet. 2006, 7:715-727.
59. Klose R.J., Yamane K., Bae Y., Zhang D., Erdjument-Bromage H., Tempst P., Wong J., Zhang Y. The transcriptional repressor JHDM3A demethylates trimethyl histone H3 lysine 9 and lysine 36. Nature 2006, 442:312-316.
60. Klose R.J., Yan Q., Tothova Z., Yamane K., Erdjument-Bromage H., Tempst P., Gilliland D.G., Zhang Y., Kaelin W.G. The retinoblastoma binding protein RBP2 is an H3K4 demethylase. Cell 2007, 128:889-900.
61. Klose R.J., Zhang Y. Regulation of histone methylation by demethylimination and demethylation. Nat. Rev. Mol. Cell. Biol. 2007, 8:307-318.
62. Kooistra S.M., Helin K. Molecular mechanisms and potential functions of histone demethylases. Nat. Rev. Mol. Cell. Biol. 2012, 13:297-311.
63. Kouzarides T. Chromatin modifications and their function. Cell 2007, 128:693-705.
64. Lee D.Y., Teyssier C., Strahl B.D., Stallcup M.R. Role of protein methylation in regulation of transcription. Endocr. Rev. 2005, 26:147-170.
65. Lee J., Thompson J.R., Botuyan M.V., Mer G. Distinct binding modes specify the recognition of methylated histones H3K4 and H4K20 by JMJD2A-tudor. Nat. Struct. Mol. Biol. 2008, 15:109-111.
66. Lee M., Norman J., Shilatifard A. ScienceDirect.com - Cell - Physical and functional association of a trimethyl H3K4 demethylase and Ring6a/MBLR, a Polycomb-like protein. Cell 2007, 128:877-887.
67. Lee M.G., Wynder C., Cooch N., Shiekhattar R. An essential role for CoREST in nucleosomal histone 3 lysine 4 demethylation. Nature 2005, 437:432-435.
68. Lee M.G., Wynder C., Schmidt D.M., McCafferty D.G., Shiekhattar R. Histone H3 lysine 4 demethylation is a target of nonselective antidepressive medications. Chem. Biol. 2006, 13:563-567.
69. Lee N., Zhang J., Klose R.J., Erdjument-Bromage H., Tempst P., Jones R.S., Zhang Y. The trithorax-group protein Lid is a histone H3 trimethyl-Lys4 demethylase. Nat. Struct. Mol. Biol. 2007, 14:341-343.
70. Li B.X., Zhang M.C., Luo C.L., Yang P., Li H., Xu H.M., Xu H.F., Shen Y.W., Xue A.M., Zhao Z.Q. Effects of RNA interference-mediated gene silencing of JMJD2A on human breast cancer cell line MDA-MB-231 in vitro. J. Exp. Clin. Canc. Res. 2011, 30:90.
71. Li W., Zhao L., Zang W., Liu Z., Chen L., Liu T., Xu D., Jia J. Histone demethylase JMJD2B is required for tumor cell proliferation and survival and is overexpressed in gastric cancer. Biochem. Biophys. Res. Commun. 2011, 416:372-378.
72. Liang G., Klose R.J., Gardner K.E., Zhang Y. Yeast Jhd2p is a histone H3 Lys4 trimethyl demethylase. Nat. Struct. Mol. Biol. 2007, 14:243-245.
73. Lim S., Janzer A., Becker A., Zimmer A., Schule R., Buettner R., Kirfel J. Lysine-specific demethylase 1 (LSD1) is highly expressed in ER-negative breast cancers and a biomarker predicting aggressive biology. Carcinogenesis 2010, 31:512-520.
74. Liu G., Bollig-Fischer A., Kreike B., van de Vijver M.J., Abrams J., Ethier S.P., Yang Z.Q. Genomic amplification and oncogenic properties of the GASC1 histone demethylase gene in breast cancer. Oncogene 2009, 28:4491-4500.
75. Lohse B., Kristensen J.L., Kristensen L.H., Agger K., Helin K., Gajhede M., Clausen R.P. Inhibitors of histone demethylases. Bioorg. Med. Chem. 2011, 19:3625-3636.
76. Lohse B., Nielsen A.L., Kristensen J.B., Helgstrand C., Cloos P.A., Olsen L., Gajhede M., Clausen R.P., Kristensen J.L. Targeting histone lysine demethylases by truncating the histone 3 tail to obtain selective substrate-based inhibitors. Angew. Chem. Int. Ed. 2011, 50:9100-9103.
77. Luo X., Liu Y., Kubicek S., Myllyharju J., Tumber A., Ng S., Che K.H., Podoll J., Heightman T.D., Oppermann U., Schreiber S.L., Wang X. A selective inhibitor and probe of the cellular functions of Jumonji C domain-containing histone demethylases. J. Am. Chem. Soc. 2011, 133:9451-9456.
78. Marks P.A., Breslow R. Dimethyl sulfoxide to vorinostat: development of this histone deacetylase inhibitor as an anticancer drug. Nat. Biotechnol. 2007, 25:84-90.
79. McDonough M.A., McNeill L.A., Tilliet M., Papamicael C.A., Chen Q.Y., Banerji B., Hewitson K.S., Schofield C.J. Selective inhibition of factor inhibiting hypoxia-inducible factor. J. Am. Chem. Soc. 2005, 127:7680-7681.
80. Metzger E., Imhof A., Patel D., Kahl P., Hoffmeyer K., Friedrichs N., Muller J.M., Greschik H., Kirfel J., Ji S., Kunowska N., Beisenherz-Huss C., Gunther T., Buettner R., Schule R. Phosphorylation of histone H3T6 by PKCbeta(I) controls demethylation at histone H3K4. Nature 2010, 464:792-796.
81. Metzger E., Wissmann M., Yin N., Muller J.M., Schneider R., Peters A.H., Gunther T., Buettner R., Schule R. LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature 2005, 437:436-439.
82. Meyer R., Wolf S.S., Obendorf M. PRMT2, a member of the protein arginine methyltransferase family, is a coactivator of the androgen receptor. J. Steroid. Biochem. Mol. Biol. 2007, 107:1-14.
83. Mimasu S., Sengoku T., Fukuzawa S., Umehara T., Yokoyama S. Crystal structure of histone demethylase LSD1 and tranylcypromine at 2.25 A. Biochem. Biophys. Res. Commun. 2008, 366:15-22.
84. Mimasu S., Umezawa N., Sato S., Higuchi T., Umehara T., Yokoyama S. Structurally designed trans-2-phenylcyclopropylamine derivatives potently inhibit histone demethylase LSD1/KDM1. Biochemistry (Mosc) 2010, 49:6494-6503.
85. Mitra D., Das P.M., Huynh F.C., Jones F.E. Jumonji/ARID1 B (JARID1B) protein promotes breast tumor cell cycle progression through epigenetic repression of microRNA let-7e. J. Biol. Chem. 2011, 286:40531-40535.
86. Mosammaparast N., Shi Y. Reversal of histone methylation: biochemical and molecular mechanisms of histone demethylases. Annu. Rev. Biochem. 2010, 79:155-179.
87. Ng H.H., Robert F., Young R.A., Struhl K. Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol. Cell. 2003, 11:709-719.
88. Ng S.S., Kavanagh K.L., McDonough M.A., Butler D., Pilka E.S., Lienard B.M., Bray J.E., Savitsky P., Gileadi O., von Delft F., Rose N.R., Offer J., Scheinost J.C., Borowski T., Sundstrom M., Schofield C.J., Oppermann U. Crystal structures of histone demethylase JMJD2A reveal basis for substrate specificity. Nature 2007, 448:87-91.
89. Nicholson T.B., Chen T. LSD1 demethylates histone and non-histone proteins. Epigenetics 2009, 4:129-132.
90. Nielsen A.L., Kristensen L.H., Stephansen K.B., Kristensen J.B., Helgstrand C., Lees M., Cloos P., Helin K., Gajhede M., Olsen L. Identification of catechols as histone-lysine demethylase inhibitors. FEBS Lett. 2012, 586:1190-1194.
91. Nimura K., Ura K., Kaneda Y. Histone methyltransferases: regulation of transcription and contribution to human disease. J. Mol. Med. 2010, 88:1213-1220.
92. Oh S., Janknecht R. Histone demethylase JMJD5 is essential for embryonic development. Biochem. Biophys. Res. Commun. 2012, 420:61-65.
93. Pollock J.A., Larrea M.D., Jasper J.S., McDonnell D.P., McCafferty D.G. Lysine-specific histone demethylase 1 inhibitors control breast cancer proliferation in ERalpha-dependent and -independent manners. ACS Chem. Biol. Article ASAP 2012, 10.1021/cb300108c.
94. Roesch A., Becker B., Schneider-Brachert W., Hagen I., Landthaler M., Vogt T. Re-expression of the retinoblastoma-binding protein 2-homolog 1 reveals tumor-suppressive functions in highly metastatic melanoma cells. J. Invest. Dermatol. 2006, 126:1850-1859.
95. Rose N.R., Ng S.S., Mecinovic J., Lienard B.M., Bello S.H., Sun Z., McDonough M.A., Oppermann U., Schofield C.J. Inhibitor scaffolds for 2-oxoglutarate-dependent histone lysine demethylases. J. Med. Chem. 2008, 51:7053-7056.
96. Rose N.R., Woon E.C., Kingham G.L., King O.N., Mecinovic J., Clifton I.J., Ng S.S., Talib-Hardy J., Oppermann U., McDonough M.A., Schofield C.J. Selective inhibitors of the JMJD2 histone demethylases: combined nondenaturing mass spectrometric screening and crystallographic approaches. J. Med. Chem. 2010, 53:1810-1818.
97. Rose N.R., Woon E.C., Tumber A., Walport L.J., Chowdhury R., Li X.S., King O.N., Lejeune C., Ng S.S., Krojer T., Chan M.C., Rydzik A.M., Hopkinson R.J., Che K., Daniel M., Strain-Damerell C., Gileadi C., Kochan G., Leung I.K., Dunford J.E., Yeoh K.K., Ratcliffe P.J., Burgess-Brown N., von Delft F., Muller S., Marsden B., Brennan P.E., McDonough M.A., Oppermann U.C., Klose R., Schofield C.J., Kawamura A. The plant growth regulator daminozide is a selective inhibitor of the human KDM2/7 histone demethylases. J. Med. Chem. Article ASAP 2012, 10.1021/jm300677j.
98. Rotili D., Altun M., Kawamura A., Wolf A., Fischer R., Leung I.K., Mackeen M.M., Tian Y.M., Ratcliffe P.J., Mai A., Kessler B.M., Schofield C.J. A photoreactive small-molecule probe for 2-oxoglutarate oxygenases. Chem. Biol. 2011, 18:642-654.
99. Sakurai M., Rose N.R., Schultz L., Quinn A.M., Jadhav A., Ng S.S., Oppermann U., Schofield C.J., Simeonov A. A miniaturized screen for inhibitors of Jumonji histone demethylases. Mol. BioSyst 2010, 6:357-364.
100. Sauvageau M., Sauvageau G. Polycomb group proteins: multi-faceted regulators of somatic stem cells and cancer. Cell Stem Cell 2010, 7:299-313.
101. Schenk T., Chen W.C., Gollner S., Howell L., Jin L., Hebestreit K., Klein H.U., Popescu A.C., Burnett A., Mills K., Casero R.A., Marton L., Woster P., Minden M.D., Dugas M., Wang J.C., Dick J.E., Muller-Tidow C., Petrie K., Zelent A. Inhibition of the LSD1 (KDM1A) demethylase reactivates the all-trans-retinoic acid differentiation pathway in acute myeloid leukemia. Nat. Med. 2012, 18:605-611.
102. Schildhaus H.U., Riegel R., Hartmann W., Steiner S., Wardelmann E., Merkelbach-Bruse S., Tanaka S., Sonobe H., Schule R., Buettner R., Kirfel J. Lysine-specific demethylase 1 is highly expressed in solitary fibrous tumors, synovial sarcomas, rhabdomyosarcomas, desmoplastic small round cell tumors, and malignant peripheral nerve sheath tumors. Hum. Pathol. 2011, 42:1667-1675.
103. Schmidt D.M., McCafferty D.G. Trans-2-Phenylcyclopropylamine is a mechanism-based inactivator of the histone demethylase LSD1. Biochemistry (Mosc) 2007, 46:4408-4416.
104. Schneider J., Shilatifard A. Histone demethylation by hydroxylation: chemistry in action. ACS Chem. Biol. 2006, 1:75-81.
105. Schofield, C.J., McDonough, M.A., Rose, N.R., Thalhammer, A., 2010. Histone lysine demethylase inhibitors; Patent No. WO 2010/043866 A2, GB.
106. Schofield, C.J., Rose, N.R., Sekirnik, R., 2011. JMJD2 Demethylase Inhibitors; Patent No. WO 2011/030108 A1, GB.
107. Schulte J.H., Lim S., Schramm A., Friedrichs N., Koster J., Versteeg R., Ora I., Pajtler K., Klein-Hitpass L., Kuhfittig-Kulle S., Metzger E., Schule R., Eggert A., Buettner R., Kirfel J. Lysine-specific demethylase 1 is strongly expressed in poorly differentiated neuroblastoma: implications for therapy. Cancer Res. 2009, 69:2065-2071.
108. Secombe J., Li L., Carlos L., Eisenman R.N. The Trithorax group protein Lid is a trimethyl histone H3K4 demethylase required for dMyc-induced cell growth. Genes Dev. 2007, 21:537-551.
109. Sedkov Y., Cho E., Petruk S., Cherbas L., Smith S.T., Jones R.S., Cherbas P., Canaani E., Jaynes J.B., Mazo A. Methylation at lysine 4 of histone H3 in ecdysone-dependent development of drosophila. Nature 2003, 426:78-83.
110. Sekirnik R., Rose N.R., Thalhammer A., Seden P.T., Mecinovic J., Schofield C.J. Inhibition of the histone lysine demethylase JMJD2A by ejection of structural Zn(II). Chem. Commun. 2009, 6376-6378.
111. Sengoku T., Yokoyama S. Structural basis for histone H3 Lys 27 demethylation by UTX/KDM6A. Genes Dev. 2011, 25:2266-2277.
112. Seward D.J., Cubberley G., Kim S., Schonewald M., Zhang L., Tripet B., Bentley D.L. Demethylation of trimethylated histone H3 Lys4 in vivo by JARID1 JmjC proteins. Nat. Struct. Mol. Biol. 2007, 14:240-242.
113. Sharma S.V., Lee D.Y., Li B., Quinlan M.P., Takahashi F., Maheswaran S., McDermott U., Azizian N., Zou L., Fischbach M.A., Wong K.K., Brandstetter K., Wittner B., Ramaswamy S., Classon M., Settleman J. A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell 2010, 141:69-80.
114. Shi Y. Histone lysine demethylases: emerging roles in development, physiology and disease. Nat. Rev. Genet. 2007, 8:829-833.
115. Shi Y., Lan F., Matson C., Mulligan P., Whetstine J.R., Cole P.A., Casero R.A. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 2004, 119:941-953.
116. Shi Y., Whetstine J.R. Dynamic regulation of histone lysine methylation by demethylases. Mol. Cell. 2007, 25:1-14.
117. Shin S., Janknecht R. Diversity within the JMJD2 histone demethylase family. Biochem. Biophys. Res. Commun. 2007, 353:973-977.
118. Sippl W., Jung M. Epigenetic Targets in Drug Discovery 2009, Wiley-VCH, Weinheim.
119. Spannhoff A., Hauser A.T., Heinke R., Sippl W., Jung M. The emerging therapeutic potential of histone methyltransferase and demethylase inhibitors. Chem. Med. Chem. 2009, 4:1568-1582.
120. Spannhoff A., Sippl W., Jung M. Cancer treatment of the future: inhibitors of histone methyltransferases. Int. J. Biochem. Cell. Biol. 2009, 41:4-11.
121. Stavropoulos P., Blobel G., Hoelz A. Crystal structure and mechanism of human lysine-specific demethylase-1. Nat. Struct. Mol. Biol. 2006, 13:626-632.
122. Strobl-Mazzulla P.H., Sauka-Spengler T., Bronner-Fraser M. Histone demethylase JmjD2A regulates neural crest specification. Dev. Cell. 2010, 19:460-468.
123. Suzuki T., Miyata N. Lysine demethylases inhibitors. J. Med. Chem. 2011, 54:8236-8250.
124. Thalhammer A., Mecinovic J., Loenarz C., Tumber A., Rose N.R., Heightman T.D., Schofield C.J. Inhibition of the histone demethylase JMJD2E by 3-substituted pyridine 2,4-dicarboxylates. Org. Biomol. Chem. 2011, 9:127-135.
125. Tiainen P., Pasanen A., Sormunen R., Myllyharju J. Characterization of recombinant human prolyl 3-hydroxylase isoenzyme 2, an enzyme modifying the basement membrane collagen IV. J. Biol. Chem. 2008, 283:19432-19439.
126. Trievel R.C. Structure and function of histone methyltransferases. Crit. Rev. Eukaryot. Gene Expr. 2004, 14:147-169.
127. Tsai M.C., Wang J.K., Chang H.Y. Tumor suppression by the histone demethylase UTX. Cell Cycle 2010, 9:2043-2044.
128. Tsukada Y., Fang J., Erdjument-Bromage H., Warren M.E., Borchers C.H., Tempst P., Zhang Y. Histone demethylation by a family of JmjC domain-containing proteins. Nature 2006, 439:811-816.
129. Ueda R., Suzuki T., Mino K., Tsumoto H., Nakagawa H., Hasegawa M., Sasaki R., Mizukami T., Miyata N. Identification of cell-active lysine specific demethylase 1-selective inhibitors. J. Am. Chem. Soc. 2009, 131:17536-17537.
130. Uemura M., Yamamoto H., Takemasa I., Mimori K., Hemmi H., Mizushima T., Ikeda M., Sekimoto M., Matsuura N., Doki Y., Mori M. Jumonji domain containing 1A is a novel prognostic marker for colorectal cancer: in vivo identification from hypoxic tumor cells. Clin. Cancer Res. 2010, 16:4636-4646.
131. Upadhyay A.K., Rotili D., Han J.W., Hu R., Chang Y., Labella D., Zhang X., Yoon Y.S., Mai A., Cheng X. An analog of BIX-01294 selectively inhibits a family of histone H3 lysine 9 Jumonji demethylases. J. Mol. Biol. 2012, 416:319-327.
132. Vinatzer U., Gollinger M., Mullauer L., Raderer M., Chott A., Streubel B. Mucosa-associated lymphoid tissue lymphoma: novel translocations including rearrangements of ODZ2, JMJD2C, and CNN3. Clin. Cancer Res. 2008, 14:6426-6431.
133. Wang J., Lu F., Ren Q., Sun H., Xu Z., Lan R., Liu Y., Ward D., Quan J., Ye T., Zhang H. Novel histone demethylase LSD1 inhibitors selectively target cancer cells with pluripotent stem cell properties. Cancer Res. 2011, 71:7238-7249.
134. Webby C.J., Wolf A., Gromak N., Dreger M., Kramer H., Kessler B., Nielsen M.L., Schmitz C., Butler D.S., Yates J.R., Delahunty C.M., Hahn P., Lengeling A., Mann M., Proudfoot N.J., Schofield C.J., Bottger A. Jmjd6 catalyses lysyl-hydroxylation of U2AF65, a protein associated with RNA splicing. Science 2009, 325:90-93.
135. Whetstine J.R., Nottke A., Lan F., Huarte M., Smolikov S., Chen Z., Spooner E., Li E., Zhang G., Colaiacovo M., Shi Y. Reversal of histone lysine trimethylation by the JMJD2 family of histone demethylases. Cell 2006, 125:467-481.
136. Willmann D., Lim S., Wetzel S., Metzger E., Jandausch A., Wilk W., Jung M., Forne I., Imhof A., Janzer A., Kirfel J., Waldmann H., Schule R., Buettner R. Impairment of prostate cancer cell growth by a selective and reversible LSD1 inhibitor. Int. J. Cancer 2012.
137. Wissmann M., Yin N., Muller J.M., Greschik H., Fodor B.D., Jenuwein T., Vogler C., Schneider R., Gunther T., Buettner R., Metzger E., Schule R. Cooperative demethylation by JMJD2C and LSD1 promotes androgen receptor-dependent gene expression. Nat. Cell. Biol. 2007, 9:347-353.
138. Woon E.C., Tumber A., Kawamura A., Hillringhaus L., Ge W., Rose N.R., Ma J.H., Chan M.C., Walport L.J., Che K.H., Ng S.S., Marsden B.D., Oppermann U., McDonough M.A., Schofield C.J. Linking of 2-oxoglutarate and substrate binding sites enables potent and highly selective inhibition of JmjC histone demethylases. Angew. Chem. Int. Ed. 2012, 51:1631-1634.
139. Xiang Y., Zhu Z., Han G., Ye X., Xu B., Peng Z., Ma Y., Yu Y., Lin H., Chen A.P., Chen C.D. JARID1B is a histone H3 lysine 4 demethylase up-regulated in prostate cancer. P. Natl. Acad. Sci. USA 2007, 104:19226-19231.
140. Xu W., Yang H., Liu Y., Yang Y., Wang P., Kim S.H., Ito S., Yang C., Xiao M.T., Liu L.X., Jiang W.Q., Liu J., Zhang J.Y., Wang B., Frye S., Zhang Y., Xu Y.H., Lei Q.Y., Guan K.L., Zhao S.M., Xiong Y. Oncometabolite 2-hydroxyglutarate is a competitive inhibitor of alpha-ketoglutarate-dependent dioxygenases. Cancer Cell 2011, 19:17-30.
141. Yamane K., Toumazou C., Tsukada Y., Erdjument-Bromage H., Tempst P., Wong J., Zhang Y. JHDM2A, a JmjC-containing H3K9 demethylase, facilitates transcription activation by androgen receptor. Cell 2006, 125:483-495.
142. Yang J., Ledaki I., Turley H., Gatter K.C., Montero J.C., Li J.L., Harris A.L. Role of hypoxia-inducible factors in epigenetic regulation via histone demethylases. Ann. NY Acad. Sci. 2009, 1177:185-197.
143. Yang M., Culhane J.C., Szewczuk L.M., Gocke C.B., Brautigam C.A., Tomchick D.R., Machius M., Cole P.A., Yu H. Structural basis of histone demethylation by LSD1 revealed by suicide inactivation. Nat. Struct. Mol. Biol. 2007, 14:535-539.
144. Yang M., Culhane J.C., Szewczuk L.M., Jalili P., Ball H.L., Machius M., Cole P.A., Yu H. Structural basis for the inhibition of the LSD1 histone demethylase by the antidepressant trans-2-phenylcyclopropylamine. Biochemistry (Mosc) 2007, 46:8058-8065.
145. Yang M., Gocke C.B., Luo X., Borek D., Tomchick D.R., Machius M., Otwinowski Z., Yu H. Structural basis for CoREST-dependent demethylation of nucleosomes by the human LSD1 histone demethylase. Mol. Cell. 2006, 23:377-387.
146. Yang Z.Q., Imoto I., Fukuda Y., Pimkhaokham A., Shimada Y., Imamura M., Sugano S., Nakamura Y., Inazawa J. Identification of a novel gene, GASC1, within an amplicon at 9p23-24 frequently detected in esophageal cancer cell lines. Cancer Res. 2000, 60:4735-4739.
147. Yoshimi A., Kurokawa M. Key roles of histone methyltransferase and demethylase in leukemogenesis. J. Cell. Biochem. 2011, 112:415-424.
148. Zhu S., Li Y., Zhao L., Hou P., Shangguan C., Yao R., Zhang W., Zhang Y., Tan J., Huang B., Lu J. TSA-induced JMJD2B downregulation is associated with cyclin B1-dependent survivin degradation and apoptosis in LNCap cells. J. Cell. Biochem.r 2012, 113:2375-2382.